Upregulation of special AT-rich-binding protein 1 by Epstein-Barr virus latent membrane protein 1 in human nasopharyngeal cells and nasopharyngeal cancer

Journal of General Virology

Volumn 94, Issue PART3, 2013, Pages 507-513

  Endo, Kazuhira ^a,b   Shackelford, Julia ^a   Aga, Mitsuharu ^a,b   Yoshizaki, Tomokazu ^b   Pagano, Joseph S ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b KANAZAWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH FACTOR; LATENT MEMBRANE PROTEIN 1; MEMBRANE PROTEIN; SHORT HAIRPIN RNA; SPECIAL AT RICH BINDING PROTEIN 1; SURVIVIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER TISSUE; CELL GROWTH; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; EPSTEIN BARR VIRUS; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; NASOPHARYNX; NASOPHARYNX CARCINOMA; ONCOGENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

CELL LINE; CELL PROLIFERATION; GENE EXPRESSION REGULATION; HERPESVIRUS 4, HUMAN; HUMANS; MATRIX ATTACHMENT REGION BINDING PROTEINS; NASOPHARYNGEAL NEOPLASMS; NOSE; PHARYNX; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; VIRAL MATRIX PROTEINS;

EID: 84874089640     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.046243-0     Document Type: Article

References (73)

1. Agrelo, R. & Wutz, A. (2009). Cancer progenitors and epigenetic contexts: an Xisting connection. Epigenetics 4, 568-570.
2. Agrelo, R., Souabni, A., Novatchkova, M., Haslinger, C., Leeb, M., Komnenovic, V., Kishimoto, H., Gresh, L., Kohwi-Shigematsu, T. & Kenner, L. (2009). SATB1 defines the developmental context for gene silencing by Xist in lymphoma and embryonic cells. Dev Cell 16, 507-516.
3. Alvarez, J. D., Yasui, D. H., Niida, H., Joh, T., Loh, D. Y. & Kohwi-Shigematsu, T. (2000). The MAR-binding protein SATB1 orchestrates temporal and spatial expression of multiple genes during T-cell development. Genes Dev 14, 521-535.
4. Arbach, H., Viglasky, V., Lefeu, F., Guinebretière, J. M., Ramirez, V., Bride, N., Boualaga, N., Bauchet, T., Peyrat, J. P. & other authors (2006). Epstein-Barr virus (EBV) genome and expression in breast cancer tissue: effect of EBV infection of breast cancer cells on resistance to paclitaxel (Taxol). J Virol 80, 845-853.
5. Bai, M., Papoudou-Bai, A., Kitsoulis, P., Horianopoulos, N., Kamina, S., Agnantis, N. J. & Kanavaros, P. (2005). Cell cycle and apoptosis deregulation in classical Hodgkin lymphomas. In Vivo 19, 439-453.
6. Brinkmann, M. M. & Schulz, T. F. (2006). Regulation of intracellular signalling by the terminal membrane proteins of members of the Gammaherpesvirinae. J Gen Virol 87, 1047-1074.
7. Burgos, J. S. (2005). Involvement of the Epstein-Barr virus in the nasopharyngeal carcinoma pathogenesis. Med Oncol 22, 113-122.
8. Cai, S., Han, H. J. & Kohwi-Shigematsu, T. (2003). Tissue-specific nuclear architecture and gene expression regulated by SATB1. Nat Genet 34, 42-51.
9. Cheng, C., Lu, X., Wang, G., Zheng, L., Shu, X., Zhu, S., Liu, K., Wu, K. & Tong, Q. (2010). Expression of SATB1 and heparanase in gastric cancer and its relationship to clinicopathologic features. APMIS 118, 855-863.
10. Cheung, C. H., Cheng, L., Chang, K. Y., Chen, H. H. & Chang, J. Y. (2011). Investigations of survivin: the past, present and future. Front Biosci 16, 952-961.
11. Church, D. N. & Talbot, D. C. (2012). Survivin in solid tumors: rationale for development of inhibitors. Curr Oncol Rep 14, 120-128.
12. Contreras-Brodin, B. A., Anvret, M., Imreh, S., Altiok, E., Klein, G. & Masucci, M. G. (1991). B cell phenotype-dependent expression of the Epstein-Barr virus nuclear antigens EBNA-2 to EBNA-6: studies with somatic cell hybrids. J Gen Virol 72, 3025-3033.
13. Dickinson, L. A., Joh, T., Kohwi, Y. & Kohwi-Shigematsu, T. (1992). A tissue-specific MAR/SAR DNA-binding protein with unusual binding site recognition. Cell 70, 631-645.
14. Fukayama, M., Hino, R. & Uozaki, H. (2008). Epstein-Barr virus and gastric carcinoma: virus-host interactions leading to carcinoma. Cancer Sci 99, 1726-1733.
15. Han, H. J., Russo, J., Kohwi, Y. & Kohwi-Shigematsu, T. (2008). SATB1 reprogrammes gene expression to promote breast tumour growth and metastasis. Nature 452, 187-193.
16. Hatzivassiliou, E. & Mosialos, G. (2002). Cellular signaling pathways engaged by the Epstein-Barr virus transforming protein LMP1. Front Biosci 7, d319-d329.
17. Hino, R., Uozaki, H., Inoue, Y., Shintani, Y., Ushiku, T., Sakatani, T., Takada, K. & Fukayama, M. (2008). Survival advantage of EBV-associated gastric carcinoma: survivin up-regulation by viral latent membrane protein 2A. Cancer Res 68, 1427-1435.
18. Horikawa, T., Yang, J., Kondo, S., Yoshizaki, T., Joab, I., Furukawa, M. & Pagano, J. S. (2007). Twist and epithelial-mesenchymal transition are induced by the EBV oncoprotein latent membrane protein 1 and are associated with metastatic nasopharyngeal carcinoma. Cancer Res 67, 1970-1978.
19. Horikawa, T., Yoshizaki, T., Kondo, S., Furukawa, M., Kaizaki, Y. & Pagano, J. S. (2011). Epstein-Barr virus latent membrane protein 1 induces Snail and epithelial-mesenchymal transition in metastatic nasopharyngeal carcinoma. Br J Cancer 104, 1160-1167.
20. Iorns, E., Hnatyszyn, H. J., Seo, P., Clarke, J., Ward, T. & Lippman, M. (2010). The role of SATB1 in breast cancer pathogenesis. J Natl Cancer Inst 102, 1284-1296.
21. Izumi, K. M. (2004). Epstein-Barr virus signal transduction and B-lymphocyte growth transformation. Prog Mol Subcell Biol 36, 269-288.
22. Kanwar, R. K., Cheung, C. H., Chang, J.-Y. & Kanwar, J. R. (2010). Recent advances in anti-survivin treatments for cancer. Curr Med Chem 17, 1509-1515.
23. Kanwar, J. R., Kamalapuram, S. K. & Kanwar, R. K. (2011). Targeting survivin in cancer: the cell-signalling perspective. Drug Discov Today 16, 485-494.
24. Kondo, S., Wakisaka, N., Schell, M. J., Horikawa, T., Sheen, T. S., Sato, H., Furukawa, M., Pagano, J. S. & Yoshizaki, T. (2005). Epstein-Barr virus latent membrane protein 1 induces the matrix metalloproteinase-1 promoter via an Ets binding site formed by a single nucleotide polymorphism: enhanced susceptibility to nasopharyngeal carcinoma. Int J Cancer 115, 368-376.
25. Kondo, S., Seo, S. Y., Yoshizaki, T., Wakisaka, N., Furukawa, M., Joab, I., Jang, K. L. & Pagano, J. S. (2006). EBV latent membrane protein 1 up-regulates hypoxia-inducible factor 1alpha through Siah1-mediated down-regulation of prolyl hydroxylases 1 and 3 in nasopharyngeal epithelial cells. Cancer Res 66, 9870-9877.
26. Kondo, S., Yoshizaki, T., Wakisaka, N., Horikawa, T., Murono, S., Jang, K. L., Joab, I., Furukawa, M. & Pagano, J. S. (2007). MUC1 induced by Epstein-Barr virus latent membrane protein 1 causes dissociation of the cell-matrix interaction and cellular invasiveness via STAT signaling. J Virol 81, 1554-1562.
27. Kondo, S., Wakisaka, N., Muramatsu, M., Zen, Y., Endo, K., Murono, S., Sugimoto, H., Yamaoka, S., Pagano, J. S. & Yoshizaki, T. (2011). Epstein-Barr virus latent membrane protein 1 induces cancer stem/ progenitor-like cells in nasopharyngeal epithelial cell lines. J Virol 85, 11255-11264.
28. Kumar, P. P., Purbey, P. K., Ravi, D. S., Mitra, D. & Galande, S. (2005). Displacement of SATB1-bound histone deacetylase 1 corepressor by the human immunodeficiency virus type 1 transactivator induces expression of interleukin-2 and its receptor in T cells. Mol Cell Biol 25, 1620-1633.
29. Kumar, P. P., Bischof, O., Purbey, P. K., Notani, D., Urlaub, H., Dejean, A. & Galande, S. (2007). Functional interaction between PML and SATB1 regulates chromatin-loop architecture and transcription of the MHC class I locus. Nat Cell Biol 9, 45-56.
30. Kuo, T. C. & Chao, C. C. (2010). Hepatitis B virus X protein prevents apoptosis of hepatocellular carcinoma cells by upregulating SATB1 and HURP expression. Biochem Pharmacol 80, 1093-1102.
31. Lam, N. & Sugden, B. (2003). CD40 and its viral mimic, LMP1: similar means to different ends. Cell Signal 15, 9-16.
32. Li, H. P. & Chang, Y. S. (2003). Epstein-Barr virus latent membrane protein 1: structure and functions. J Biomed Sci 10, 490-504.
33. Li, K., Cai, R., Dai, B. B., Zhang, X. Q., Wang, H. J., Ge, S. F., Xu, W. R. & Lu, J. (2007). SATB1 regulates SPARC expression in K562 cell line through binding to a specific sequence in the third intron. Biochem Biophys Res Commun 356, 6-12.
34. Lippert, B. M., Knauer, S. K., Fetz, V., Mann, W. & Stauber, R. H. (2007). Dynamic survivin in head and neck cancer: molecular mechanism and therapeutic potential. Int J Cancer 121, 1169-1174.
35. Lladser, A., Sanhueza, C., Kiessling, R. & Quest, A. F. (2011). Is survivin the potential Achilles' heel of cancer? Adv Cancer Res 111, 1-37.
36. Lo, A. K., Liu, Y., Wang, X. H., Huang, D. P., Yuen, P. W., Wong, Y. C. & Tsao, G. S. (2003). Alterations of biologic properties and gene expression in nasopharyngeal epithelial cells by the Epstein-Barr virus-encoded latent membrane protein 1. Lab Invest 83, 697-709.
37. Lu, X., Cheng, C., Zhu, S., Yang, Y., Zheng, L., Wang, G., Shu, X., Wu, K., Liu, K. & Tong, Q. (2010). SATB1 is an independent prognostic marker for gastric cancer in a Chinese population. Oncol Rep 24, 981-987.
38. Lu, J., Murakami, M., Verma, S. C., Cai, Q., Haldar, S., Kaul, R., Wasik, M. A., Middeldorp, J. & Robertson, E. S. (2011). Epstein-Barr virus nuclear antigen 1 (EBNA1) confers resistance to apoptosis in EBV-positive B-lymphoma cells through up-regulation of survivin. Virology 410, 64-75.
39. Mainou, B. A., Everly, D. N., Jr & Raab-Traub, N. (2007). Unique signaling properties of CTAR1 in LMP1-mediated transformation. J Virol 81, 9680-9692.
40. Margulis, V., Lotan, Y. & Shariat, S. F. (2008). Survivin: a promising biomarker for detection and prognosis of bladder cancer. World J Urol 26, 59-65.
41. Marquitz, A. R. & Raab-Traub, N. (2012). The role of miRNAs and EBV BARTs in NPC. Semin Cancer Biol 22, 166-172.
42. McGuire, B. B. & Fitzpatrick, J. M. (2009). Biomarkers in renal cell carcinoma. Curr Opin Urol 19, 441-446.
43. Meng, W. J., Yan, H., Zhou, B., Zhang, W., Kong, X. H., Wang, R., Zhan, L., Li, Y., Zhou, Z. G. & Sun, X. F. (2012). Correlation of SATB1 overexpression with the progression of human rectal cancer. Int J Colorectal Dis 27, 143-150.
44. Mori, F., Piro, F. R., Della Rocca, C., Mesiti, G., Giampaoli, S., Silvestre, G. & Lazzaro, D. (2007). Survivin and Cyclooxygenase-2 are co-expressed in human and mouse colon carcinoma and in terminally differentiated colonocytes. Histol Histopathol 22, 61-77.
45. Morris, M. A., Dawson, C. W. & Young, L. S. (2009). Role of the Epstein-Barr virus-encoded latent membrane protein-1, LMP1, in the pathogenesis of nasopharyngeal carcinoma. Future Oncol 5, 811-825.
46. Murono, S., Inoue, H., Tanabe, T., Joab, I., Yoshizaki, T., Furukawa, M. & Pagano, J. S. (2001). Induction of cyclooxygenase-2 by Epstein-Barr virus latent membrane protein 1 is involved in vascular endothelial growth factor production in nasopharyngeal carcinoma cells. Proc Natl Acad Sci U S A 98, 6905-6910.
47. Pagano, J. (2009). EBV Diseases. In DNA Tumor Viruses, pp 217-240. New York: Springer.
48. Patani, N., Jiang, W., Mansel, R., Newbold, R. & Mokbel, K. (2009). The mRNA expression of SATB1 and SATB2 in human breast cancer. Cancer Cell Int 9, 18.
49. Pavan Kumar, P., Purbey, P. K., Sinha, C. K., Notani, D., Limaye, A., Jayani, R. S. & Galande, S. (2006). Phosphorylation of SATB1, a global gene regulator, acts as a molecular switch regulating its transcriptional activity in vivo. Mol Cell 22, 231-243.
50. Paydas, S., Ergin, M., Seydaoglu, G., Erdogan, S. & Yavuz, S. (2009). Prognostic [corrected] significance of angiogenic/lymphangiogenic, anti-apoptotic, inflammatory and viral factors in 88 cases with diffuse large B cell lymphoma and review of the literature. Leuk Res 33, 1627-1635.
51. Peng, Z. K., Yang, D. H., Li, X. H., Huang, Y., Zhang, G. Q., Zhong, K. B., Bi, M. P. & Li, G. H. (2011). [Expression of special AT-rich sequence-binding protein 1 mRNA in hepatocellular carcinoma and its clinical significance]. Nan Fang Yi Ke Da Xue Xue Bao 31, 1207-1211. (in Chinese).
52. Savarese, F., Dávila, A., Nechanitzky, R., De La Rosa-Velazquez, I., Pereira, C. F., Engelke, R., Takahashi, K., Jenuwein, T., Kohwi-Shigematsu, T. & other authors (2009). Satb1 and Satb2 regulate embryonic stem cell differentiation and Nanog expression. Genes Dev 23, 2625-2638.
53. Shi, W., Bastianutto, C., Li, A., Perez-Ordonez, B., Ng, R., Chow, K. Y., Zhang, W., Jurisica, I., Lo, K. W. & other authors (2006). Multiple dysregulated pathways in nasopharyngeal carcinoma revealed by gene expression profiling. Int J Cancer 119, 2467-2475.
54. Shushan, S., Cinamon, U., Levy, D., Sokolov, M. & Roth, Y. (2009). Laryngeal cancer in acquired immunodeficiency syndrome. Int J STD AIDS 20, 582-584.
55. Slovin, S. F., Glassy, M. C., Dambaugh, T., Catalano, M. A., Curry, R. A., Ferrone, S., Kieff, E., Vaughan, J. H. & Carson, D. A. (1981). Discordant expression of 2 Epstein-Barr virus-associated antigens, EBNA and RANA, in man-rodent somatic cell hybrids. J Immunol 127, 585-590.
56. Soni, V., Cahir-McFarland, E. & Kieff, E. (2007). LMP1 TRAFficking activates growth and survival pathways. Adv Exp Med Biol 597, 173-187.
57. Sun, Y., Wang, T., Su, Y., Yin, Y., Xu, S., Ma, C. & Han, X. (2006). The behavior of SATB1, a MAR-binding protein, in response to apoptosis stimulation. Cell Biol Int 30, 244-247.
58. Takimoto, T., Sato, H., Ogura, H., Tanaka, S. & Umeda, R. (1988). The difference in tumorigenicity between Epstein-Barr virus (EBV) genome-positive and genome-negative epithelial hybrid cell lines derived from the human nasopharynx. Laryngoscope 98, 1334-1338.
59. Tsao, S. W., Tramoutanis, G., Dawson, C. W., Lo, A. K. & Huang, D. P. (2002a). The significance of LMP1 expression in nasopharyngeal carcinoma. Semin Cancer Biol 12, 473-487.
60. Tsao, S. W., Wang, X., Liu, Y., Cheung, Y. C., Feng, H., Zheng, Z., Wong, N., Yuen, P. W., Lo, A. K. & other authors (2002b). Establishment of two immortalized nasopharyngeal epithelial cell lines using SV40 large T and HPV16E6/E7 viral oncogenes. Biochim Biophys Acta 1590, 150-158.
61. Tu, W., Luo, M., Wang, Z., Yan, W., Xia, Y., Deng, H., He, J., Han, P. & Tian, D. (2012). Upregulation of SATB1 promotes tumor growth and metastasis in liver cancer. Liver Int 32, 1064-1078.
62. Wakisaka, N. & Pagano, J. S. (2003). Epstein-Barr virus induces invasion and metastasis factors. Anticancer Res 23 (3A), 2133-2138.
63. Wakisaka, N., Murono, S., Yoshizaki, T., Furukawa, M. & Pagano, J. S. (2002). Epstein-Barr virus latent membrane protein 1 induces and causes release of fibroblast growth factor-2. Cancer Res 62, 6337-6344.
64. Wakisaka, N., Kondo, S., Yoshizaki, T., Murono, S., Furukawa, M. & Pagano, J. S. (2004). Epstein-Barr virus latent membrane protein 1 induces synthesis of hypoxia-inducible factor 1 alpha. Mol Cell Biol 24, 5223-5234.
65. Wen, J., Huang, S., Rogers, H., Dickinson, L. A., Kohwi-Shigematsu, T. & Noguchi, C. T. (2005). SATB1 family protein expressed during early erythroid differentiation modifies globin gene expression. Blood 105, 3330-3339.
66. Yasui, D., Miyano, M., Cai, S., Varga-Weisz, P. & Kohwi-Shigematsu, T. (2002). SATB1 targets chromatin remodelling to regulate genes over long distances. Nature 419, 641-645.
67. Yoshizaki, T., Sato, H., Furukawa, M. & Pagano, J. S. (1998). The expression of matrix metalloproteinase 9 is enhanced by Epstein-Barr virus latent membrane protein 1. Proc Natl Acad Sci U S A 95, 3621-3626.
68. Yoshizaki, T., Wakisaka, N. & Pagano, J. S. (2005). Epstein-Barr virus: Invasion and Metastasis. Norfolk, UK: Caister Academic Press.
69. Zhang, Q., Zhang, Z., Wang, C., Xiao, Z., Yu, Y., Yang, F., Chen, Z. & He, Z. (2008a). Proteome analysis of the transformation potential of the Epstein-Barr virus-encoded latent membrane protein 1 in nasopharyngeal epithelial cells NP69. Mol Cell Biochem 314, 73-83.
70. Zhang, R., Wang, T., Li, K. N., Qin, W. W., Chen, R., Wang, K., Jia, L. T., Zhao, J., Wen, W. H. & other authors (2008b). A survivin double point mutant has potent inhibitory effect on the growth of hepatocellular cancer cells. Cancer Biol Ther 7, 547-554.
71. Zhao, X. D., Ji, W. Y., Zhang, W., He, L. X., Yang, J., Liang, H. J. & Wang, L. L. (2010). Overexpression of SATB1 in laryngeal squamous cell carcinoma. ORL J Otorhinolaryngol Relat Spec 72, 1-5.
72. Zheng, J. (2008). Is SATB1 a master regulator in breast cancer growth and metastasis? Womens Health (Lond Engl) 4, 329-332.
73. Zheng, H., Li, L. L., Hu, D. S., Deng, X. Y. & Cao, Y. (2007). Role of Epstein-Barr virus encoded latent membrane protein 1 in the carcinogenesis of nasopharyngeal carcinoma. Cell Mol Immunol 4, 185-196.